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Scientific Status Summary Parasites and the Food Supply

This Scientific Status Summary, prepared for the Institute of Food Technologists’ Expert Panel on Food Safety and Nutrition, discusses the sources and incidence of by foodborne parasites and the new technologies that are being developed for their prevention, detection, and inactivation.

Palmer A. Orlandi, Dan-My T. Chu, atterns of travel, trade in foods and food consumption have Jeffrey W. Bier and George J. Jackson changed, exposing consumers to pathogens—including Pparasitic — not previously encountered. The globaliza- tion of America’s food supply increased substantially during the 1990s (Fig. 1). Correspondingly, so did the risk to American consumers of acquiring a foodborne parasite. In 1990, about 13 of parasitic animals were of concern to food scientists in the United States (Jackson, 1990). Today, that figure has multiplied by more than a factor of 8. In the past, the risk of human infection with parasites was considered to be limited to distinct geographic regions because of parasites’ adapta- tions to specific definitive hosts, select intermediate hosts and particular environmental conditions. These barriers are slowly being breeched—first by international travel developing into a major industry, and then by rap- id, refrigerated food transport which became available to an unprecedent- ed degree at the end of the 20th century. Figs. 2A and B trace the numbers of international travelers to and from All authors are or were with the Center for Food Safety and the U.S. over the past decade and provide further projections for interna- Applied Nutrition, Food and Drug Administration, College tional travel through 2003. International travel and population migration Park, MD 20740-3835. Palmer Orlandi is a biochemical are the primary mechanisms by which immunologically naive (previously unexposed) consumers may come into contact with emerging parasites. parasitologist in the Office of Applied Research and Safety Another factor to consider is the rapid transport of foreign food prod- Assessment. Dan-My Chu is a parasitologist in the Office of ucts to the U.S., which has further enhanced the chances that parasites Plant, Dairy Foods and Beverages. Jeff Bier is a parasitolo- come into contact with consumers. Now, produce picked and seafood har- gist and consultant, formerly with the Office of Seafood. vested or caught early in the week, thousands of miles from our borders, George Jackson is a parasitologist in the Office of Science can be consumed fresh in America’s heartlands before the weekend. More- and the Dean of the Center for Food Safety and Applied over, cultural habits have shifted toward the consumption of fresh, i.e., raw Nutrition’s Staff College. and undercooked, foods that bypass important preparatory measures in-

72 FOODTECHNOLOGY APRIL 2002 • VOL. 56, NO. 4 tended to reduce or prevent by 1990; Taylor and Baker, 1978) and, for lence in temperate and arctic climates. pathogens—especially the long-surviving forms encysted on or within plant or Domestically, for a multitude of rea- encysted forms of foodborne parasites. tissues, our inability to design sons, parasitic infections are often not Food is an emerging seeding experiments that are equivalent routinely considered as a source of ill- discipline. Although its beginnings coin- to working with natural samples. ness when symptoms similar to bacterial cided with the beginnings of microscopy Frequently, parasitology in its entire- infection present themselves. Therefore, more than 300 years ago (Dobell, 1920), ty is relegated to the status of a sub-spe- many instances of parasite-related ill- few of its testing methods are as stan- cialty in between microbiology and zo- ness go undiagnosed, which may lead to dardized as those of food bacteriology. ology. Moreover, pathogenic parasites of a skewed reporting of the incidences of Reasons for the underdeveloped state of are sometimes considered only parasitic illness. As a consequence, those this science include our inability to in the context of tropical medicine, de- parasites that are now considered readily culture most parasites (Smyth, spite mounting evidence of their preva- emerging parasitic pathogens may in fact have been a continual source of hu- man illness in the absence of any clinical recognition. In the context of foods and parasitic animals, then, there is a need for in- creased awareness of the impact of para- sites on the food supply. This includes recognition of parasites’ potential effect on public health and health care issues as well as sensitivity to economic conse- quences such as worker productivity and agricultural losses. In comparison to other classes of foodborne pathogens, particularly bacteria, the impact of par- asites is difficult to assess primarily due to the lack of a uniform standard for monitoring the incidence of foodborne Fig. 1—Value of agricultural products imported into the United States. From USDC (2000a). illness directly attributed to parasitic in- fection. As such, statistical data relating parasitic and econom- A ic sequelae are either approximations or lacking.

Scope of the Problem There are about 107 known species of parasitic animals that can be food- borne (Table 1). While not all species are reported to infest domestic food sources or infect consumers in the U.S. and its territories, the likelihood of this possibility has significantly increased in recent years with the emergence of a truly global market place. Planetary sta- tistics on foodborne illnesses due to par- asitic infections have been difficult to es- B timate. Norman R. Stoll’s classic “This Wormy World” (Stoll, 1947) estimated that in the global population of 2.2 bil- lion people, there were 664 million As- caris lumbricoides infections (30% prev- alence) and 355 million infections with trichiura (16%) compared to the update by Michael et al. (1997) which estimated 1273 million (24%) and 902 million (17%) infections 50 years later when the human population was 5.6 billion. What percentage of these cases is foodborne has not been determined; however, their overall im- Fig. 2—International travel (A) to the U.S. and (B) from the U.S. From USDC (2000b). pact as demonstrated by substantial in-

VOL. 56, NO. 4 • APRIL 2002 FOODTECHNOLOGY 73 Scientific Status Summary

Table 1—Parasites transmitted by food and water cidences of foodborne trem- atode infections (Opistorchis, Geographic Key feature/ Clonorchis) in Southeast Parasite Stage Pathogenicity Sourcea areab food/hosts and the Pacific region (WHO, 1995) underscores PROTISTA the need for increased awareness of this class of hu- Amoebae man pathogens. Particularly Endolimax nana Cyst _ W,F,H U with the consumption of Entamoeba chattoni Cyst _ W,F,H U raw or undercooked seafood Entamoeba coli Cyst _ W,F,H U and the advent of a global Entamoeba dispar Cyst _ W,F,H U Entamoeba invadens Cyst _ W,F,H U market place, the need for Entamoeba hartmanni Cyst _ W,F,H U precautions in processing Cyst + W,F,H U May invade methods and consumption extraintestinal sites habits is essential to prevent Entamoeba moshkovskii Cyst _ W,F,H U Morphologically the spread of foodborne par- similar to E. hystolytica asitic infections. This aware- Entamoeba polecki Cyst ± W,F,H U , monkey ness also applies to food-re- reservoirs Iodamoeba butschlii Cyst _ W,F,H U Pigs, monkey lated illnesses caused by gas- reservoirs trointestinal protozoa, al- though statistics comparable Flagellates to those for are not Chilomastix mesnili Cyst _ W,F,H U available. Dientamoeba fragilis Trophozoite ± H U No cyst known In the U.S., the latest sur- Enteromonas hominis Cyst _ W,F,H U Rare vey of foodborne illnesses by (lamblia) intestinalis Cyst + W,F,H U Many alternate hosts the Centers for Disease Con- Pentatrichomonas hominis Trophozoite ± W,H U Retortamonas intestinalis Cyst _ W? U Uncommon trol and Prevention esti- Retortamonas sinensis Cyst ± W C mates that there are 2.5 mil- lion cases annually due to Ciliates food- and beverage-borne Balantidium coli Cyst + W,F,H U reservoirs parasites (Mead et al., 1999). This is approximately 7% of Sporozoa and Coccidia the annual food- and bever- Cryptosporidium parvum Oocyst + W,F,H U Many hosts, cider, and age-borne disease incidence bivalve molluscs caused by known infectious Cyclospora cayetanenesis Oocyst + W,F,H? U Travel? Seasonal? Fresh produce agents—fewer than the 13% Isospora belli Oocyst ± W,F,H U More common in caused by bacteria and the tropics 80% caused by viruses. Sarcocystis hominis Cyst + F Beef intermediate However, the parasite Toxo- Sarcocystis spp. Oocyst + W,F A Sources unknown plasma gondii, a coccidian Sarcocystis suihominis Cyst + W,F Pig intermediate host protozoa, is responsible for Toxoplasma gondii Oocyst + W,F U Severe illness in fetus 20.7% of foodborne Encephalocytozoon cuniculi Spore + U U Immune-compromised humans due to known infectious Encephalocytozoon hellem Spore + U U Immune-compromised agents. The flagellated pro- humans tozoa, Giardia (lamblia) in- Encephalocytozoon Spore + U U Immune-compromised testinalis, causes the greatest intestiniale humans number of parasite-related Enterocytozoon bieneusi Spore + U U Immune-compromised disease cases, with an esti- humans mated 2,000,000 illnesses METAZOA annually, equaling 1.4% of the food- and beverage- borne total for known Achillurbainia recondita Metacercaria + F C pathogenic agents. Alaria americana Metacercaria + F NA Frogs Cryptosporidium parvum is Appophalus donicus Metacercaria + F reported to cause 30,000 Artyfechinostomum mehrai Metacercaria + F I Fish cases (0.2%) and the recent- Centrocestus spp. Metacercaria + F AS Fish, eggs may enter ly recognized Cyclospora cay- circulation etanensis caused 14,638 cases Centrocestus formosanus Metacercaria + F AS Fish, eggs may enter circulation (0.1%), due primarily to im- ᭤ ported fresh produce. Al- a Source: W = water, F = food, H = food handler though it is difficult to dis- b Geographic area: U = Ubiquitous, A = , AS = Asia, C = , E =Egypt, I = , , IN = Indonesia, H = Hawaii, HA = Holartic, J = Japan, NA = North America, SA = South America, SEA = South East Asia, O = Orient, P = Phillipines, R = Russia, US = United States. tinguish foodborne from

74 FOODTECHNOLOGY APRIL 2002 • VOL. 56, NO. 4 Table 1—Parasites transmitted by food and water, continued waterborne illnesses attrib- uted to these species, their Geographic Key feature/ impact on food safety and Parasite Stage Pathogenicity Sourcea areab food/hosts public health both nationally Metacercaria + F CJ Fish and internationally appears Cryptocotyle lingua Metacercaria + F Fish to be significant (Käferstein, Metacercaria + F U Vegetables, ant 2000). transport host The relationship between Diorchitrema formosenum Metacercaria + F Fish, eggs may enter enteric parasitic protozoa, circulation the environment, contami- Diorchitrema pseudocirratum Metacercaria + F Fish, eggs may enter nation of food, and human circulation Diorchitrema spp. Metacercaria + F Fish, eggs may enter illness is extremely complex. circulation Environmental factors play a Echinochasmus spp. Metacercaria + F Fish significant role in the trans- Echinoparyphium Metacercaria + F U Fish mission of most foodborne recurvatum parasitic diseases. This im- Echinostoma iliocenum Metacercaria + F P , clams pact is particularly apparent Echinostoma lindoensi Metacercaria + F I reservoirs, molluscs with protozoa, which are Echinostoma revoltum Metacercaria + F U Snails, clams readily transported to food Echinostoma spp. Metacercaria + F A Molluscs by contaminated water (Slif- Episthmium caninum Metacercaria + F Fish ko et al., 2000a). Fecal con- Euparyphium melis Metacercaria + F Fish tamination of water sources Eurytrema pancreaticum Metacercaria + F O Fish, can occlude used in crop irrigation, food pancreas gigantica Metacercaria + F ME Vegetables processing and meal prepa- Metacercaria + F U Sheep reservoir, ration are important sources vegetables of human infection. In this buski Metacercaria + F AS Pig reservoir, regard, contamination of vegetables fresh fruits and vegetables is Fischoederius elongatus Metacercaria + F Vegetables causing the greatest concern. hominis Metacercaria + F AS Vegetables These commodities are inti- Gymnophalloides seoi Metacercaria + F K Fish? Haplorchis spp. Metacercaria + F Fish, eggs may enter mately influenced by the en- circulation vironment and agricultural Metacercaria + F U Mullet primary vector practices, and often receive Heterophyes nocens Metacercaria + F AS Fish, eggs may enter no processing that is lethal to circulation protozoa. Heterophyopsis continua Metacercaria + F U Fish, eggs may enter The deployment of more circulation Himasthla muehlensi Metacercaria + F US Clams efficient and rapid means of Hypoderaeum conoideum Metacercaria + F Fish transporting perishable Isoparorchis hypselobagri Metacercaria + F Fish, man accidental goods worldwide enables host fresh produce to be available Metagonimus minutus Metacercaria + F Fish, eggs may enter in the U.S. nearly year- circulation round. Together, these fac- Metacercaria + F AS,E Fish Nanophyetus salmincola Metacercaria + F NA Fish (California to tors have influenced the British Columbia) emergence and recognition Nanophyetus schikhobalowi Metacercaria + F R Fish (Siberia) of some parasites as new hu- Neodiplostomum seoulensis Metacercaria + F K Snakes man pathogens. viverrini Metacercaria + F SEA Fish Cryptosporidium parvum Metacercaria + F Fish and Cyclospora cayetanensis, Paragonimus spp. Metacercaria + F U Fish Paryphostomum surfrartyfex Metacercaria + F I Unknown intermediate for example, rapidly became hosts important human pathogens Phagicola spp. Metacercaria + F Fish in the U.S. during the 1980s Phaneropsolus bonnei Metacerceria + F SEA Fish and 1990s, infecting immu- Plagiorchis spp. Metacercaria + F U intermediate nocompromised and immu- Poikilorchis congolensis Metacercaria + F A Fish? nocompetent individuals Procerovum spp. Metacercaria + F Fish alike. While not generally as- Prohemistomum vivax Metacercaria + F E Prosthodendrium Metacercaria + F Fish sociated with human disease molenkampi earlier in the 20th century, C. Pygidiopsis summa Metacercaria + F SEA Fish parvum and C. cayetanensis Stellantchasmus spp. Metacercaria + F AS Fish are now frequently identified Stellantchasmus falcatus Metacercaria + F O,H Fish as causative agents in human Stictodora fuscata Metacercaria + F Fish illness. Additionally, each is Watsonius watsoni Metacercaria + F A Vegetables, monkey alternate host ᭤ linked epidemiologically to

VOL. 56, NO. 4 • APRIL 2002 FOODTECHNOLOGY 75 Scientific Status Summary

Table 1—Parasites transmitted by food and water, continued the consumption of fresh produce in both sporadic Geographic Key feature/ and clustered outbreaks Parasite Stage Pathogenicity Sourcea areab food/hosts (Table 2). Although both these protozoa can be food- studeri Plerocercoid _ F?W? AS Mite intermediate host borne pathogens, it is highly Braunia jasseyensis Plerocercoid + F AS Probably transmitted likely that they are more of- by fish ten waterborne organisms latum Plerocercoid + F U Fish, pernicious and transmitted to humans by environmental factors Diphyllobothrium spp Plerocercoid + F U Fish and agricultural practices. Diplydium caninum Plerocercoid + F?,W? U , mainly infants Diplogonoporus grandis Plerocercoid + F?W? U Crustacea, normal The microsporidia, another host whales rapidly emerging group of Digramma brauni Plerocercoid + F Fish human pathogens, may also granulosus Egg + F,W,H U Picnics belong in this category. Echinococcus multilocularis Egg + F,W,H U Picnics Although the contribu- Egg + F,W,H U Picnics tion of these protozoan par- dimunita Egg + F,W,H U Fleas Hynenelepis nana Egg + F,W,H U Fleas asites to overall foodborne Inermicapsifer illness, as reflected in recent madagascariensis Egg? + F,W,H A Unknown life cycle statistics (Mead et al., 1999), Plerocercoid _ F Unknown life cycle appears to be small, it is spp. Plerocercoid + F Unknown flesh highly likely that the num- Multiceps multiceps Egg + F,W U bers are underestimates. demerariensis Plerocercoid + F sp. Procercoid? + F Fish Spirometra erinacei Plerocercoid + F Fish Analytical Methods serialis Egg + F,W,H Methods for the detection Taenia multiceps Egg + F,W U of food- and water-borne Taenia saginatta + F U Cows parasites have expanded Cysticercoid/Egg + F U Pigs, autochthonous from traditional microscopic Taenia spp. Cysticercoid + F U techniques to include such molecular tools as the poly- Bulbosoma spp. Juvenile + F R Fish merase chain reaction (PCR) Corynosoma strumosum Juvenile + F R Fish and species-specific immu- nologically-based assays. Nematoda Whereas morphological duodenale + F U Vegetables identification of worms (hel- spp. Larva + F U Fish minths) and protozoan Angiostrongylus Larva + F,W U Vegetables pathogens remains a vital as- cantonensis pect of analysis, molecular Angiostrongylus Larva + F,W NA,SA Vegetables costaricensis and sometimes immunologic Egg + F,W U Vegetables diagnoses are rapidly being hepatica Larva + F U Vegetables incorporated as more sensi- Capillaria philippinensis Larva + F P Fish tive standard practices. Capillaria spp. Larva + F NA,SA Fish? Detection and identifica- Contracaecum sp. Larva + F U Fish tion of tissue-encysted or en- Larva + F U Fish Dracucculus medinensis Larva + W A Near eradication capsulated helminths rely Echinocehpalus sp. Larva + F U Shellfish heavily on morphological Enterobius vermicularis Egg ± F,W,H U Mainly children characterization by visual in- spp. Larva + F U Molluscs? spection and use methods Larva + F AS Reptiles, birds ranging from direct tissue Mammomonogamus spp. Egg + F,W T Vegetables? examination to mechanical Porrocaecum spp. Larva + F U Fish and enzymatic tissue disrup- Pseudoterranova spp. Larva + F U Fish Rhabditis sp. Larva _ F,W U Vegetables tion. Candling is still the Syphacia obvelata Egg ± F,W U Vegetables standard practice for detect- Toxocara cati Egg + F,W U Vegetables ing and recovering anisakid Egg + F,W U Vegetables in fish flesh (Bier nativa Larva + F HA Wild animals et al., 1995). This method Trichinella pseudospiralis Larva + F U Wild animals can be applied to fresh or Larva + F U Domestic animals Trichinella spp. Larva + F U Wild animals frozen white-fleshed fish that Egg + F,W U Vegetables are processed as fillets, spp. Larva + F U Vegetables steaks, or minced fish. Using a “cool white” light source,

76 FOODTECHNOLOGY APRIL 2002 • VOL. 56, NO. 4 the appearance of parasitic worms may Visual examination is the predomi- parvum is linked to such criteria as oo- vary from reddish to a chalky white. A nant method of inspection for the pres- cyst size, shape, and sporulation charac- similar procedure using reflected long- ence of the cysticerci (larval forms) of teristics (Goodgame, 1996). Staining wave ultraviolet light (366 nm) in which Taenia solium ( tapeworm) in pig and autofluorescent properties (such as the ’s larval stages fluoresce blue carcasses and (beef tape- those of C. cayetanensis) further distin- or green may be used for fish with dark worm) in bovine carcasses. Post-mor- guish these parasites, although, these flesh (Brattey, 1988). Compression can- tem macroscopic inspection of selective means of identification are complicated dling is applied to such translucent muscle tissue is the primary means of by variability in staining patterns foods as shellfish. Alternatively, tissue detecting these parasites, although en- (Negm, 1998; Visvesvera et al.,1997). In- disruption is highly effective in liberat- zyme-acid digestion of tissue similar to efficient isolation and concentration ing parasites for easier identification that used to examine fish is also em- techniques—used to counteract small and establishing accurate counts. The ployed (Arambulo, 1982). Ante-mortem size, low numbers, and the large sample simple technique of homogenizing fish detection methods using serological sizes required—create additional prob- flesh in a food processor and inspecting tests are currently available. Although lems for analyses that already are labori- the diluted debris under shortwave UV hemagluttination tests show some ous and time-consuming. Additionally, light is an efficient means of detecting promise, these and other procedures as in all microscopic diagnoses, identifi- larval anisakid nematodes of the genera have demonstrated variable specificity cation is highly dependent on the skill, Anisakis and Phocanema (Brattey, 1988). and sensitivity and may not be practical experience and expertise of the micros- Alone or in combination with saline due to high cost. Additionally, a host’s copist (Goodgame, 1996). elution or pepsin-HCl (enzyme acid) di- weak immunological response to light While microscopy remains an impor- gestion of the homogenate, this ap- infections may complicate definitive di- tant diagnostic component for definitive proach offers the investigator a greater agnoses. identification of protozoan parasites, degree of parasite recovery. Using these In the past, detection and identifica- newer techniques are more sensitive, types of disruptive methods, the whitish tion of pathogenic protozoa from water specific, and time-efficient. PCR proto- plerocercoids of Dyphyllobothrium spp. sources and foods were equally depen- cols for Cyclospora and Cryptosporidium (larval tapeworms) can also be more dent on traditional microscopy. Howev- detection have been used successfully easily recovered and identified (Aramb- er, success with microscopy has proven over the last several years for clinical, ulo, 1982). Metacercaria and mesocer- to be much more difficult for protozoa environmental and, more recently, food caria (larval forms of trematodes) are than for the helminths. Definitive mi- surveys (Rose and Slifko, 1999). These also more easily detected and identified croscopic identification of coccidian protocols include methods to differenti- with the aid of these methods. parasites such as C. cayetanensis and C. ate among species or closely related gen- era. To distinguish between C. cayetan- ensis and Eimeria spp., PCR products Table 2—Foodborne outbreaks associated with parasites also must be examined either by restric- tion fragment length polymorphism Food item(s) analysis (RFLP) (Jinneman et al., 1998) Infection Parasite implicated/associated Reference or an oligonucleotide ligation assay (OLA) (Jinneman et al., 1999). Amebiasis Entamoeba Ice cream, fruit de Lalla et al. (1992) histolytica With the recent description of several Cyclospora-like species isolated from Anisakiasis Anisakis Raw saltwater fish Machi et al. (1997) non-human primates (Eberhard et al., Raw fish Muraoka et al. (1996) 1999; Lopez et al., 1999; Smith et al., 1996), a new nested PCR protocol, capa- Ascaris lumbricoides Imported vegetables Raisanen et al. (1985) ble of differentiating C. cayetanenesis Cryptosporidiosis Cryptosporidium Chicken salad CDC (1996b) from related non-human parasites (Or- parvum landi, 2001) is currently under develop- Cryptosporidium Green onions CDC (1998) ment at the U.S. Food and Drug Admin- istration (FDA). Cyclosporiasis Cyclospora Basil Lopez et al. (2001) Molecular techniques provide con- cayetanensis Raspberries Caceres et al. (1998) siderable advances in detection sensi- Dessert Fleming et al. (1998) tivity, specificity and ease of analysis. Diphyllobothrium Salmon Ruttenber et al. (1984) These methods, however, still depend on our ability to isolate and concen- Fascioliasis Fasciola hepatica Lettuce Espino et al. (1998) trate the parasite from the sample ma- trix and prepare a suitable DNA tem- Giardiasis Giardia lamblia Raw sliced vegetables Mintz et al. (1993) plate free of matrix-derived substances Fruit salad Porter et al. (1990) that may inhibit PCR. An extraction- Nanophyetiasis Nanophyetus Salmonid fish Eastburn et al. (1987) free, filter-based method of preparing salmincola DNA templates now exists for the PCR detection of such protozoa as C. cayet- Trichinellosis Trichinella Horse meat Ancelle et al. (1998) anensis, C. parvum, and the various mi- Cougar jerky CDC (1996b) crosporidia genera and species in a va-

VOL. 56, NO. 4 • APRIL 2002 FOODTECHNOLOGY 77 Scientific Status Summary riety of complex matrices (foods, envi- Control Measures Mixtures of chemicals such as the in- ronmental samples, and clinical speci- Contamination of food products by situ generation of mixed oxidants, may mens) (Orlandi and Lampel, 2000). parasites may occur at several points be more effective than a single chemical, This protocol increased the sensitivity along the path from growing and har- such as chlorine, which does not inacti- of PCR detection and alleviated the vesting food at the farm or fishing vate protozoan cysts and oocysts (Venc- need for time-consuming purification grounds to consumption by the con- zel et al., 1997). schemes that can contribute to signifi- sumer. Possible contamination sources Consumer preferences for the con- cant sample losses and affect detection include the use of parasite contaminated sumption of fresh fruits and vegetables sensitivity. The protocol was successful- irrigation or spraying water, contamina- preclude the use of heat as a control ly used to identify C. cayetanensis as a tion of surfaces during harvesting or measure against parasitic contamina- contaminant in a chicken-basil-pasta processing, and contamination of food tion. Application of cold temperatures salad implicated in a 1999 outbreak of products during final preparation and may serve as a useful alternative: freez- cyclosporiasis in Missouri (Lopez et al., packaging. Furthermore, certain geno- ing C. parvum to –20°C and –70°C ren- 2001). types of C. parvum, T. gondii and G. in- dered oocysts noninfectious and nonvi- In addition to PCR, several immuno- testinalis have reservoir hosts that in- able after 24 and 1 hr, respectively (Fayer logically-based assays were developed crease their frequency in the environ- and Nerad, 1996). FDA’s “Fish and Fish- for C. parvum. Monoclonal ment and thereby their threat to public eries Products Hazards and Controls to oocyst surface antigens are currently health. Guide” recommends that raw fish available for use in immunofluorescence A number of control measures are served for consumption should be fro- microscopy or as a component in com- used to protect food products from par- zen at either (1) –35°C (or below) until mercial (enzyme-linked-immune-sor- asites. Foremost among the traditional solid and stored at –35°C or below for bent assay) kits. Immunomagnetic sepa- measures are the cleaning and cooking 15 hr, (2) –35°C (or below) until solid ration techniques are also being refined of food items prior to consumption. and stored at –20°C (or below) for at and applied as a means of isolating, con- Most parasites’ heat resistance is not im- least 24 hr, or (3) –20°C or below for 7 centrating, and purifying C. parvum oo- pressive, and temperatures as low as 56– days (total time) prior to being sold cysts from complex matrices. No com- (FDA, 2001). Proper freezing of fish mercially available immunological re- products destroys helminths capable of agents currently exist for C. cayetanensis. Protozoa . . . are now causing disease after consumption of Whereas molecular methods have such raw fish dishes as , sashimi, or provided a means for rapid and sensi- among the dominant ceviche. Freezing, particularly in the tive detection of parasites in foods, the short term, however is unpredictable— question of whether those organisms public health concerns in freezing can inactivate parasites but un- detected in complex matrices are viable der certain conditions also may preserve and therefore infective still remains. several nations and can them. Animal infectivity studies, where possi- Water serves as an important vehicle ble (i.e., C. parvum, G. intestinalis), cause disease outbreaks for of foodborne parasites. provide the most definitive answer to that encompass entire In developed nations, treatment of pub- the question of viability in comparison lic water sources with halogenated com- to sporulation, excystation, and tissue communities. pounds, predominantly chlorine, signif- culture models (in vitro studies). How- icantly reduces the public health threat ever, animal infectivity studies are labo- of bacterial pathogens such as Vibrio rious, time-consuming, and expensive 60°C for several minutes will, in many cholerae. Protozoa such as G. intestinalis (Neumann et al., 2000). instances, eliminate the infectivity of and the coccidia that are resistant to an- Deng et al. (1997) proposed an al- helminths (Fayer et al., 2001). Heating tibacterial levels of chlorine are now ternative method using immunomag- to > 72°C for 1 min or 45°C for 10–20 among the dominant public health con- netic capture PCR to distinguish viable min inactivates C. parvum oocysts cerns in several nations and can cause and dead C. parvum. In addition, via- (Steiner et al., 1997). However, the heat disease outbreaks that encompass entire bility stain assessment and fluorescent must uniformly penetrate the entire communities. in situ hybridization studies have also food matrix because parasites such as Furthermore, the Environmental proved useful (Deere et al., 1998; Neu- Trichinella or Anisakis may be encysted Protection Agency standard for water mann et al., 2000; Vesey et al., 1998). deep inside the tissues. quality is based on a total bacterial For other parasitic protozoa such as Other processes, used primarily for coliform count (EPA, 1990). This crite- Cyclospora and the microsporidia, the preparation and preservation of fish rion does not appear to be a reliable in- where genetic and surface antigen in- are effective in inactivating helminths. dicator for parasite contamination of formation is lacking, assessment of via- These include hot smoking, fermenta- water. This was apparent during the bility remains difficult. Sporulation, tion in brine, and drying (WHO, 1995); 1993 C. parvum outbreak in Milwaukee, excystation (e.g., Cyclospora) and spore cold smoking and salting, however, may in which the implicated water source germination in conjunction with tissue not be effective against fishborne met all federal quality standards (Mac culture infectivity (e.g., microsporidia) anisakid nematodes. Cleaning methods Kenzie et al., 1994). Filtration of water are currently the only method for include such actions as peeling, washing also has improved water quality, al- gauging viability (Ortega et al., 1998; or scrubbing fresh produce that is usual- though the small size of some parasites Wittner and Weiss, 1999). ly contaminated at or near the surface. may allow their passage through certain

78 FOODTECHNOLOGY APRIL 2002 • VOL. 56, NO. 4 types of filters. An absolute 1-µ filter is radiation on food products. Guatemalan raspberries, the MPE has required to exclude Cryptosporidium. Hydrostatic pressure is a recently the potential to serve as a model policy A number of parasite control mea- proposed means by which we may be document for other produce-trading sures are being considered and evaluated able to decontaminate foods. Studies by partners to limit the risk of contaminat- for food processing (Rose and Slifko, Slifko et al. (2000a) demonstrated that ing crops with other pathogens (Calvin 1999). Ozone is a powerful oxidizing more than 99% of C. parvum oocysts in et al., 2000). agent and has been suggested as a possi- apple and orange juice were inactivated ble disinfectant for some parasites. following > 60 sec high hydrostatic Conclusions Treatment of Cryptosporidium parvum pressure treatment. The use of hydro- In the past, in the U.S., consideration in ozone-demand-free buffered H2O static pressure on fish for inactivation of of parasitic animals as foodborne with 1 ppm ozone for 5 min decreased helminths is currently being investigat- pathogens waned with the incorpora- both oocyst excystation and infectivity ed. While some of the control measures tion of better food handling and sanita- to mice by greater than 90% (Korich et discussed exhibit efficacy against certain tion practices, and inspection proce- al., 1990). parasites, none of these procedures has dures. However, events during the latter Ozone inactivation, however, is de- been demonstrated to be as uniformly part of the 20th century forced us to fo- pendent on a number of parameters in- reliable as heat. cus again on the potential health risks cluding temperature, medium pH, and Control measures used to decontam- posed by parasitic protozoa and helm- the amount of extracellular organic inate food products once contaminated inths. Globalization of food trade, pref- matter residing around the parasite; by parasites are only one intervention to erences for raw and undercooked dishes, therefore, penetration of ozone into prevent human illness caused by the in- ease of international travel, and increas- food crevices where parasites may reside gestion of foods harboring parasitic ing numbers of immunocompromised may not occur (Kim et al., 1999). pathogens. Surveillance programs are individuals are factors that have contrib- Irradiation serves as another possible another means to control and limit the uted to the increase in foodborne para- measure for parasite control. UV irradi- impact of foodborne parasites on public sitic infections. This is further compli- ation, as a method for inactivating health. Such programs can serve as ef- cated by the emergence of parasites not Cryptosporidium in apple cider, is cur- fective indicators of potential contami- previously associated with pathogenesis rently being investigated. Preliminary nation problems through periodic test- in humans. results demonstrate a 5-log10 reduction ing. Though somewhat costly, surveil- Educational outreach and research in oocyst viability (Hanes, 2001). lance of those foods, such as fresh pro- programs developed through the U.S. Whereas UV irradiation has the poten- duce, previously identified as “at-risk” government’s Food Safety Initiative have tial to serve as an efficient method for for parasitic contamination acts to pro- been relatively successful in increasing inactivation of Cryptosprodium for tect both the producer and the consum- public awareness of food safety issues even small producers, its economic fea- er and minimize the risk of large food- and potential health risks (FSI, 2001). sibility has yet to be determined. borne outbreaks. A step towards such a Nevertheless, it is probable that the inci- Ionizing irradiation is effective in surveillance program is the development dence of illness attributed to parasitic controlling helminths such as and implementation of policies, similar contamination of food and water is un- , Anisakis simplex, to seafood HACCP, designed to limit, derreported. The reasons for the under- Clonorchis sinensis, and Paragonimus control, and monitor sources of parasite reporting are: the lack of recognition of westermani (Venugopal et al., 1999). In contact with food. potential effects of parasite contamina- the control of Trichinella spiralis-infect- In an effort to preserve the raspberry tion on public health and the absence of ed pork, FDA approved the use of irra- industry in Guatemala in 1999, the routine screening protocols for these diation at an absorbed dose of 0.3 kGy- Model Plan of Excellence (MPE) was pathogens. 1.0 kGy (FDA, 1985). While ionizing ir- developed through the cooperative ef- With the emphasis on food safety radiation is useful for inactivation of a forts of the U.S. Food and Drug Admin- continuing and food security being a number of parasites, it does not uni- istration, the Guatemalan government, major concern since September 11, formly inactivate all parasites to the and the Guatemalan Berry Commission 2001, the development of new technolo- same degree; a considerable range in the to guard berries intended for export gies for the prevention, detection and log reduction is reported (Enigk et al., against contamination with C. cayetan- inactivation of foodborne parasites is 1975). ensis. The MPE is a strict version of being accelerated. In conjunction with Also, inactivation of parasites may Good Agricultural Practices and is in- an increased awareness of the health require a range of doses because the ef- tended to decrease the risk of contami- risks associated with parasitic contami- fectiveness of the process is dependent nating crops with Cyclospora. As a sys- nation and illness, the control of food- on the parasite, the stage of the parasite tem designed to monitor many food borne parasites is expected to become that has contaminated the food matrix, safety aspects of farming, it provides for more effective. and the types and characteristics of the oversight and surveillance of food matrix itself (Farkas, 1998). practices, water source development, ir- REFERENCES Hence, many parameters must be ex- rigation methods, food handling, and Ancelle, T., Dupouy-Camet, J., Desenclos, J.C., Maillot, amined before irradiation will become employee hygiene. 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80 FOODTECHNOLOGY APRIL 2002 • VOL. 56, NO. 4 gov/view/f-2000-99-001/trend2003.html. Venczel, L.V., Arrowood, M., Hurd, M., and Sobsey, M.D. 1997. Inactivation of Cryptosporidium parvum oocysts and Clostridium perfringens spores by a mixed-oxidant disinfectant and by free chlorine. App. The Society for Food Science and Technology Environ. Microbiol. 63: 1598-1601. World Headquarters: 525 W. Van Buren Street, Suite 1000, Chicago, IL 60607 Venugopal, V., Doke, S.N., and Thomas, P. 1999. Radi- ation processing to improve the quality of fishery Voice: 312–782–8424 • Fax: 312–782–8348 products. Crit. Rev. Food Sci. Nutr. 39(5): 391-440. e-mail: [email protected] • www.ift.org Vesey, G., Ashbolt, N., Fricker, E.J., Deere, D., Williams, Washington, D.C.: 1025 Connecticut Ave., NW, Suite 503, Washington, DC 20036 K.L., Veal, D.A., and Dorsch, M. 1998. The use of a Voice: 202–466–5980 • Fax: 202–466–5988 ribosomal RNA targeted oligonucleotide probe for flu- e-mail: [email protected] • www.ift.org orescent labeling of viable Cryptosporidium parvum oocysts. J. Appl. Microbiol. 85: 429-440. Visvesvara, G., Moura, H., Kovacs, Nace, E., Wallace, S. Scientific Status Summaries are published in Food Technology by the Institute of Food Technologists’ Expert and Eberhard, M.L. 1997. Uniform staining of Cy- clospora oocysts in fecal smears by a modified safra- Panel on Food Safety and Nutrition. IFT’s Expert Panel on Food Safety and Nutrition, which studies signifi- nin technique with microwave heating. J. Clin. Micro- cant food-related issues and oversees timely production of Scientific Status Summaries, comprises acade- biol. 35: 730-733. micians representing expertise in one or more areas of food science/technology and nutrition. Scientific Wittner, M., Weiss.and L.M. 1999. “The Microsporidia Status Summaries, which are not necessarily written by the Expert Panel, are rigorously peer-reviewed by and Microsporidiosis.” ASM Press, Washington, D.C. the Expert Panel as well as by individuals outside the panel who have specific expertise in the subject. WHO. 1995. Control of foodborne trematode infections. WHO Tech. Rept. Series. No. 849, pp. 1-157 World The Scientific Status Summaries may be reprinted or photocopied without permission, provided that suit- ● Health Organization, Rome. able credit is given.

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